AWA: Academic Writing at Auckland

The primate sensory and motor systems are astoundingly well organised, exhibiting remarkable similarities in the way in which the brain codes for very different stimuli. Consequently, understanding the properties of the visual system, such as such as coarse coding, retinotopic organisation, cortical magnification, contralateral representation, differential coupling and division of labour, can lead to understanding other sensory and motor systems.

An effective sensory system must be able to differentiate between vast numbers of stimuli, and indeed the primate visual system is capable of identifying millions of objects, their size and their location. Hypothetically, the visual cortex could contain millions of finely-tuned neurons, each responding solely to a specific stimulus, and indeed the olfactory system does exhibit this one to one method of identification. The visual system, however, relies on the property of coarse coding to encode numerous stimuli using relatively few neurons (Purves et al., 2008). Coarse coding is extremely significant as it provides an efficient and elegant method of coding an infinite variety of stimuli using a finite (and often very small) number of neurons that is used throughout the brain.

According to this model, the responses of multiple neurons to aspects of the stimulus are combined to allow identification of that stimulus as a whole. The most well-known example of coarse coding, the Young-Helmholtz theory of colour vision, was also one of the first theories to incorporate this property (Erickson, 2001). According to this model, there are three types of retinal cone photoreceptors, each of which responds best to a different range of wavelengths of light. Analysis of human eyes surgically removed due to malignant growths has since revealed that there are in fact three types of cones, with absorbance peaks at 558.4 ± 5.2 nm, 530.8 ± 3.5 nm and 419.0 ± 3.6 nm respectively (Dartnall, Bowmaker & Mollon, 1983). Despite only responding to three broad ranges of wavelengths of light (popularly but inaccurately conceptualised as red, green and blue), humans experience many shades of colour due to coarse coding. It is the ratio of activation of the different types of cones, rather than the number of cones, that allows the perception of subtle gradations of colour.

Coarse coding is a useful tool for maximising the efficiency of neurons in the visual system, so it is no surprise that examples of this property can be found in sensory and motor systems. For example, neurons of the superior colliculus use coarse coding to control saccadic eye movement (Lee, Rohrer, & Sparks, 1988). In this case, it is the vector sum of the activation of multiple neurons with large receptive fields that codes the direction of the resulting eye movement. Similarly, multiple broadly-tuned neurons of the primate motor cortex are activated together in specific patterns to produce fine movements (Georgopoulos, Schwartz, Ketiner, 1986).

Not only must a sensory system identify objects, it must code for their position relative to other objects. In the visual system, the preservation of spatial information is achieved by retinotopic organisation throughout the brain areas involved in vision.  Initially, images of objects are projected through the lens and onto the retina in much the same fashion as an image on the film of a pinhole camera. Retinal ganglia then project up to the lateral geniculate nucleus and on to the striate cortex, all the while retaining their position relative to each other. As such, the image on the retina is transcribed to the visual cortices, its spatial organisation preserved in several distinct retinotopic maps (Engel, Glover, & Wandell, 1997).

Interestingly, despite this retinotopic organisation, the cortex does not always contain a to-scale map of the world. Instead, cortical magnification occurs, allowing visual information from the centre of the visual fields to occupy more cortical space than information from the periphery (Pointer, 1986). This ensures that the most important visual information, that which the individual is fixating on, receives sufficient space for maximum processing.

The principles of retinotopic organisation and cortical magnification can be generalised to many primate somatosensory and motor systems. Perhaps the best-known example is the somatotopic mapping that occurs in the primary sensory and motor cortices. That is, all the neurons concerned with the hand are located together, as are all the neurons associated with the nose, and so on to form a somatotopic map (Penfield & Rasmussen, 1950). Interestingly, this map appears to reflect foetal rather than adult orientation of the body in space: the hands are mapped next to the face, and the feet next to the genitals, as those body parts are arranged in the foetal position (Farah, 1998). As in the visual system, multiple topographic maps of the body occur in the primary motor and sensory cortices; for example, the primary sensory cortex of the owl monkey contains four complete somatotopic maps (Merzenich, Kaas, Sur, & Lin, 1978).

Cortical magnification is clearly apparent in cartoon representations of the motor and sensory cortices in the form of homunculi whose proportions are distorted compared to those of a normal human body. For example, in the motor cortex the hands (which have many muscles and frequently perform fine, coordinated movements) are overrepresented, and the genitals (which are far less involved in movement) are underrepresented. In contrast, in the sensory cortex both the hands and genitals are overrepresented, as both produce a lot of sensory output (Schott, 1993).  

The degree of magnification associated with each body part appears to be affected by use. For example, the area of the right motor cortex corresponding to the left digits is larger in musicians who play string instruments than in other people, and those musicians who took up their instrument at an early age displayed greater cortical representation (Elbert, Pantev, Wienbruch, Rockstroh& Taub, 1995). This provides further evidence that those areas that are magnified in the cortex are those areas that are used: string players must be able to make many rapid, fine, coordinated motor movements with their left hand fingers on the fingerboard of their instrument if they are to perform successfully.

The opposite case occurs in people who have had a limb amputated. Over time, the parts of the cortex responsible for sensing and controlling movement of body parts adjacent to the lost limb on the sensorimotor homunculus will expand into the unused region that once controlled the amputated limb, reducing the area of ‘wasted space’ in the cortex (Knecht et al., 1995). The overrepresentation of important motor and sensory body parts in the motor and somatosensory cortices is directly analogous to the overrepresentation of the central few degrees of vision in the visual cortices.

Unlike the visual, motor and somatosensory systems, which use topographic maps to preserve spatial organisation, the primate auditory system does not represent sound localisation on the cortex. Instead, the auditory cortex is arranged tonotopically, mapping the frequency of sounds. These maps appear to be linked to finely graded frequency perceptions in the cochlea just as the retinotopic maps in the occipital lobe are linked to fine spatial representations on the retina. Investigations using functional magnetic resonance imaging (fMRI) and a wide range of stimulus frequencies have shown that there are at least six separate tonotopic maps in the human temporal lobe (Talavage et al., 2004, for example). These maps appear to be arranged in different directions; for example, high frequencies are mapped posteriorly in the primary auditory cortex, but anteriorly in adjacent secondary auditory areas (Wessinger, Buonocore, Kussmaul & Mangun 1997).

Interestingly, there is as yet no evidence of cortical magnification in the tonotopic maps of the human auditory cortex. Instead, it seems that the cochlea projects directly on to the auditory map (Romani, Williamson, & Kaufman, 1982). This could be because the cochlea’s logarithmic frequency scale is inherently most sensitive to the most important frequencies for hearing, so no further magnification is required in the cortex.

It is well known that the primate brain has two hemispheres, and that visual information is processed in the contralateral hemisphere. This means that the left side of visual space (the left hemifields of both eyes) is mapped on to the right primary visual cortex while the right side of visual space is mapped onto the left primary visual cortex (Gratton, 1998). Capozzoli (1995) offers a detailed hypothesis as to why this contralateral representation occurs. He posits that the inversion (both vertical and horizontal) of visual stimuli that occurs at the lens is the fundamental reason for contralateral organisation. Due to this inversion, and the fact that primates have two eyes and therefore two retinal maps of visual space, information from the right visual field must cross to the left hemisphere via the optic chiasm and vice versa if that information is to be mapped logically on what he describes as the ‘cyclopean eye’ of the two occipital lobes.

It appears that visual memories are also represented contralaterally. In one visual memory experiment, Gratton, Corballis and Jain (1997) presented subjects with visual stimuli in one or the other visual field. In the next phase of the experiment, the subjects were presented with further stimuli, and asked to identify whether they had seen them before. It was found that participants were considerably more likely to accurately identify stimuli if they were presented to the same visual hemifield as they were in the first phase of the experiment. Further evidence for the contralateral representation of visual memories comes from the final part of that same study, in which event related potentials (ERPs) were recorded, for example, on the left side of the head when a stimulus was presented centrally that had originally been presented to the right visual field. These results suggest that the property of contralateral representation of visual space has flow-on effects on memory. This finding is significant as it demonstrates firstly that contralateral organisation is more far-reaching than simple visual perception, and also that memory traces are linked to the area of the brain that was involved in perceiving the initial stimulus that created the memory.

The property of contralateral representation can be generalised across primate sensory and motor systems, excepting the olfactory system. For example, decussations in the spinal column cause axons carrying information from the right motor cortex to innervate muscles on the left side of the body (Purves et al., 2008). Capozzoli (1995) suggests that contralateral motor control is a result of contralateral representation of visual information, which in turn is a result of the optical inversions that occur as light from a stimulus passes through the lens and on to the retina. Certainly, there is no immediately obvious reason why the motor system should be controlled contralaterally. However, if this system evolved alongside the contralaterally-represented visual system, then the advantages are clear. Having the left-hand side of the body represented in the same hemisphere as the left visual field allows for rapid transfer of information from the visual cortex to the motor cortex. This in turn ensures that the organism is able to respond efficiently to visual stimuli, for example by flicking its left leg to dislodge an insect sighted in the left visual field.

Imagined movements also appear to be controlled contralaterally. Johnson (1998) provides evidence for this statement by showing that subjects are able to determine which grip to use on a rapidly-presented dowel more quickly if the dowel is presented to the hemisphere contralateral to the hand they are imagining gripping with. Further evidence for contralateral control of motor imagery comes from the success of orthotic limbs controlled by electroencephalogram (EEG) signals emanating from contralateral sensorimotor areas (for example, Pfurtscheller & Neuper, 2001). The existence of coherent contralateral representation of motor imagery and visual memory, as well as actual motor control and visual perception, suggests that at least some of the same neural processes are involved in the conception and remembrance of an activity as for actually doing that activity.

If an organism is to be able to respond effectively to environmental stimuli, its sensory and motor neurons must be able to respond to change. Differential coupling is the notion that the nervous system is programmed to detect regions or times of changing stimulation. The visual system is central to primates’ ability to avoid predators and other dangerous stimuli, so it is unsurprising that this sensory system contains many examples of differential coupling. One such example of a population of neurons exhibiting differential coupling is orientation-selective cells in the striate cortex, used in the perception of edges.

Early work in this area showed that cats responded best to moving lines whose orientations were such that the line fell initially on exclusively inhibitory regions, then on excitatory regions, then again onto inhibitory regions (Hubel & Wiesel, 1962). This is evidence of differential coupling, whereby the existence of aligned ‘on’ (excitatory) and ‘off’ (inhibitory) receptive fields of neurons in the striate cortex allow the perception of changes in contrast. The ability to perceive sharp changes in contrast is functionally significant, as edge detection is an important part of identifying objects. Later studies have confirmed the existence of similar differential coupling in the striate cortices of macaque monkeys (Hubel & Wiesel, 1968, for example).

Differential coupling occurs in all sensory modalities, one example being the mammalian olfactory system. The glomerulus contains a number of interconnected glomerular units, each responding maximally to a range of chemical signals. It might therefore be assumed that olfaction is a non-specific sense, but the interconnectedness of the glomerulus means that lateral inhibition occurs between nearby glomerular units. This allows the detection of specific chemical signals, and hence the identification of individual odours (Yokoi, Mori, & Nakanishi, 1995).

Each sensory system must encode numerous aspects of each stimulus in order to make sense of it, and it seems that each aspect is processed by a different group of neurons within each system. This division of labour keeps information about one aspect of a stimulus separate from information about other aspects. In the visual system, for example, colour and motion are processed in segregated streams, each specialised for its own function.

Motion is sensed through the magnocellular pathway, involving L, M and S cones which synapse with diffuse bipolar cells, which then synapse with parasol cells whose axons project to magnocellular cells in the lateral geniculate nucleus (LGN). From the LGN, magnocellular cell axons project to spiny stellate cells of the 4Cα sublayer and finally to the blobs layer of the primary visual cortex (Nieuwenhuys, Voogd, & Huijzen, 2008). The parvocellular pathway ascends from P-type ganglion cells, through the parvocellular layers of the LGN, to the 4Cβ layer, and finally to the blobs and interblobs of the visual cortex. Parvocellular cells receive excitatory and inhibitory input from retinal cones, synthesising the relative activation of short, medium and long wavelength cones to code specific colours. In contrast, the magno cells do not receive and are unable to code colour information. They can, however, transmit action potentials far more rapidly than parvo cells, and are more sensitive to contrast, suggesting that they are specialised for coding movement and broad details (Livingstone & Hubel, 1988). Thus information regarding colour and motion is kept segregated in two specialised pathways throughout the visual system.

Functional specialisation allows for increased efficiency of sensory perception, as each specialised sub-system is adapted for its specific task. As such, it is unsurprising that the division of labour noted in the visual system should be able to be generalised to other sensory systems. In the human auditory system, for example, spectral and temporal variation (analogous to the musical elements of pitch and rhythm) are processed separately. PET data of healthy participants’ cerebral blood flow secondary to perception of changing pitch and rhythm showed that Heschl’s gyrus was active for temporal perception while the anterior superior temporal gyri and right superior temporal sulcus were active for spectral perception (Zatorre & Belin, 2001). These findings are in keeping with studies of patients with focal temporal lobe lesions who suffer from an inability to perceive pitch or rhythm, depending on the location of the lesion (Robin, Tranel, & Damasio, 1990).

In the motor system, division of labour between dorsal and ventral parts of the premotor cortex allow primates to successfully perform a motor action in response to a visual stimulus. The combined results of numerous lesion and unit-recording studies suggest that the dorsal premotor cortex is specialised for integrating information about the task at hand and determining which arm should be used, while the ventral premotor cortex receives spatial information about the target (Hoshi & Tanji, 2004). It is not yet known whether the cells of the dorsal and ventral parts are inherently different, or whether the functional specialisation observed is solely a result of differing connections to other parts of the motor and visual cortices. Either way, though the significance of division of labour in this part of the motor system is clear, further investigation is required to fully understand the extent of functional specialisation.  

Humans and indeed all organisms must possess exceptionally well-organised sensory and motor systems if they are to successfully perceive and respond to the many complex stimuli presented by the world. It is clear that the primate visual system’s properties of coarse coding, retinotopic organisation, cortical magnification, contralateral representation, differential coupling, and division of labour are instrumental in allowing that system to function effectively. Investigation into other sensory and motor systems often shows analogous functions; it appears that these properties are shared by multiple systems to produce a coherent and efficient overall sensorimotor system.

 

 

 

 

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